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Serotonin-immunoreactive neurons in the antennal lobes of the American cockroach Periplaneta americana: light- and electron-microscopic observations

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Summary

A large deutocerebral serotonin-immunoreactive neuron arborizes profusely in the glomeruli of the antennal lobes, and also sends neurites into the lateral lobe and the calyces of the mushroom bodies in the ipsilateral protocerebrum. Electron micrographs of the glomerular neuropil show that the main synapses of the serotonin-immunoreactive arborizations are output contacts with unidentified neuron profiles. Only a few synaptic input contacts with serotonin-labeled fibers were observed.

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References

  • Beaudet A, Descarries L (1987) Ultrastructural identification of serotonin neurons. In: Steinbusch HWM (ed) Monoaminergic neurons: light microscopy and ultrastructure. Wiley, Chichester, pp 265–313

    Google Scholar 

  • Belin MF, Nanopoulos D, Didier M, Aguera M, Steinbusch H, Verhofstad A, Maitre M, Pujol JF (1983) Immunohistochemical evidence for the presence of γ-aminobutyric acid and serotonin in one nerv cell. A study on the raphe nuclei of the rat using antibodies to glutamate decarboxylase and serotonin. Brain Res 275:329–339

    Google Scholar 

  • Bishop CA, O'Shea M (1983) Serotonin-immunoreactive neurons in the central nervous system of an insect (Periplaneta americana). J Neurobiol 14:251–269

    Google Scholar 

  • Bobillier P, Seguin S, Deguerce A, Lewis BD, Pujol JF (1979) The efferent connections of the nucleus raphe centralis superior in the rat as revealed by radioautography. Brain Res 166:1–8

    Google Scholar 

  • Boeckh J, Distler P, Ernst KD, Hösl M, Malun D (1990) Olfactory bulb and antennal lobe. In: Schild D (ed) Chemosensory information processing. Springer, Berlin Heidelberg New York, pp 201–228

    Google Scholar 

  • Breidbach O (1990) Serotonin-immunoreactive brain interneurons persist during metamorphosis of an insect: a developmental study of Tenebrio molitor, L. (Coleoptera). Cell Tissue Res 259:345–360

    Google Scholar 

  • Cottrell GA (1976) Does the giant cerebral neurone of Helix release two transmitters: acetylcholine and serotonin? J Physiol 259:44

    Google Scholar 

  • Davis NT (1985) Serotonin-immunoreactive visceral nerves and neurohemal system in the cockroach Periplaneta americana (L.). Cell Tissue Res 240:593–600

    Google Scholar 

  • Descarries L, Beaudet A, Watkins KC (1975) Serotonin nerve terminals in adult rat neocortex. Brain Res 100:563–588

    Google Scholar 

  • Distler P, Hösl M, Boeckh J (1986) Projection of antennal chemo- and mechanoreceptors of known functions in the supra- and the suboesophageal ganglia of the American cockroach. Verh Dtsch Zool Ges 79:269

    Google Scholar 

  • Distler P (1989) Histochemical demonstration of GABA-like immunoreactivity in cobalt labeled neuron individuals in the insect olfactory pathway. Histochemistry 91:245–249

    Google Scholar 

  • Distler P (1990a) Synaptic connections of dopamine-immunoreactive neurons in the antennal lobes of Periplaneta americana. Colocalization with GABA-like immunoreactivity. Histochemistry 93:401–408

    Google Scholar 

  • Distler P (1990b) GABA-immunohistochemistry as a label for identifying types of local interneurons and their synaptic contacts in the antennal lobes of the American cockroach. Histochemistry 93:617–626

    Google Scholar 

  • Elekes K, Hustert R, Geffard M (1987) Serotonin-immunoreactive and dopamine-immunoreactive neurons in the terminal ganglion of the cricket, Acheta domestica: light-and electron-microscopic immunocytochemistry. Cell Tissue Res 250:167–180

    Google Scholar 

  • Elekes K, Hustert H (1988) The efferent innervation of the genital chamber by an identified serotonergic neuron in the female cricket Acheta domestica. Cell Tissue Res 252:449–457

    Google Scholar 

  • Ernst KD, Boeckh J, Boeckh V (1977) A neuroanatomical study on the organization of the central antennal pathways in insects. Cell Tissue Res 176:285–308

    Google Scholar 

  • Ernst KD, Boeckh J (1983) A neuroanatomical study on the organization of the central antennal pathways in insects. Cell Tissue Res 229:1–22

    Google Scholar 

  • Evans PD (1980) Biogenic amines in the insect nervous system. Adv Insect Physiol 15:317–473

    Google Scholar 

  • Falck B, Hillarp NA, Thieme G, Torp A (1962) Fluorescence of catecholamines and related components condensed with formaldehyde. J Histochem Cytochem 10:348

    Google Scholar 

  • Halasz N, Ljungdahl A, Hökfelt T (1978) Transmitter histochemistry of the rat olfactory bulb. II. Fluorescence histochemical, autoradiographic and electron microscopic localization of monoamines. Brain Res 154:253–271

    Google Scholar 

  • Halasz N, Shepherd GM (1983) Neurochemistry of the vertebrate olfactory bulb. Neuroscience 10:579–619

    Google Scholar 

  • Hökfelt T, Johansson O, Ljungdahl A, Lundberg J, Schultzberg M (1980) Peptidergic neurones. Nature 284:515–521

    Google Scholar 

  • Homberg U, Hildebrand JG (1989a) Serotonin-immunoreactive neurons in the median protocerebrum and suboesophageal ganglion of the sphinx moth Manduca sexta. Cell Tissue Res 258:1–24

    Google Scholar 

  • Homberg U, Hildebrand JG (1989b) Serotonin immunoreactivity in the optic lobes of the sphinx moth Manduca sexta and colocalization with FMRFamide and SCPB immunoreactivity. J Comp Neurol 288:243–253

    Google Scholar 

  • Homberg U, Christensen TA, Hildebrand JG (1989) Structure and function of the deutocerebrum in insects. Ann Rev Entomol 34:477–501

    Google Scholar 

  • Hoskins SG, Homberg U, Kingan TG, Hildebrand JG (1986) Immunoreactivity of GABA in the antennal lobes of the sphinx moth Manduca sexta. Cell Tissue Res 244:243–252

    Google Scholar 

  • Hoyle G (1985) Neurotransmitters, neuromodulators and neurohormones. In: Gilles R, Balthazart J (eds) Neurobiology current comparative approaches. Springer, Berlin Heidelberg New York, pp 264–279

    Google Scholar 

  • Katz PS, Harris-Warrick RM (1989) A new role for proprioceptive feedback to CPGS: neuromodulation by serotonergic/cholinergic mechano-sensory afferents to the stomatogastric ganglion of crabs. In: Erber J, Menzel R, Pflüger HJ, Todt D (eds) Neural mechanisms of behavior. Proceedings of the 2nd International Congress of Neuroethology. Thieme, Stuttgart (no. 229)

    Google Scholar 

  • Kent KS, Hoskins SG, Hildebrand JG (1987) A novel serotonin-immunoreactive neuron in the antennal lobe of the sphinx moth Manduca sexta persists throughout postembryonic life. J Neurobiol 18:451–465

    Google Scholar 

  • Klemm N (1976) Histochemistry of putative transmitter substances in the insect brain. Prog Neurobiol 7:99–169

    Google Scholar 

  • Klemm N (1980) Histochemical demonstration of biogenic monoamines (Falck-Hillarp Method) in the insect nervous system. In: Strausfeld NJ, Miller TA (eds) Neuroanatomical techniques — Insect nervous system. Springer, Berlin Heidelberg New York, pp 51–73

    Google Scholar 

  • Klemm N, Steinbusch HWM, Sundler F (1984) Distribution of serotonin-containing neurons and their pathways in the supraoesophageal ganglion of the cockroach Periplaneta americana (L.) as revealed by immunocytochemistry. J Comp Neurol 225:387–395

    Google Scholar 

  • Kraus D, Malun D, Waldow U, Boeckh J (1988) Tracts between the deuto- and protocerebrum in the male Periplaneta americana and distribution, fine structure and connections of terminals of identified deutocerebral projection neurons. In: Elsner N, Barth FG (eds) Sense organs. Interfaces between environment and behavior. Proceedings of the 16th Göttingen Neurobiology Conference. Thieme, Stuttgart (no. 62)

    Google Scholar 

  • Lindvall O, Björklund A, Falck B (1981) Fluorescence microscopy of biogenic monoamines. In: Lahne R (ed) Methods in neurobiology, vol. 2. Plenum Press, New York London, pp 365–431

    Google Scholar 

  • Luppa H (1986) II. Prinzipien immunhistochemischer Methoden. In: Graumann W, Neumann K (eds) Handbuch der Histochemie, Band IV, Proteine Teil 2. Fischer, Stuttgart

    Google Scholar 

  • Lutz EM, Tyrer NM (1988) Immunohistochemical localization of serotonin and choline acetyltransferase in sensory neurones of the locust. J Comp Neurol 267:335–342

    Google Scholar 

  • Mercer AR (1987) Biogenic amines in the bee brain. In: Menzel R, Mercer AR (eds) Neurobiology and behavior of honeybees. Springer, Berlin Heidelberg New York, pp 244–252

    Google Scholar 

  • Nässel DR, Meyer EP, Klemm N (1985) Mapping and ultrastructure of serotonin-immunoreactive neurons in the optic lobes of three insect species. J Comp Neurol 232:190–204

    Google Scholar 

  • Nässel DR (1987) Serotonin and serotonin-immunoreactive neurons in the nervous system of insects. Prog Neurobiol 30:1–85

    Google Scholar 

  • Osborne NN (1983) Evidence for co-transmission by specific neurons. In: Osborne NN (ed) Dale's principle and communication between neurons. Pergamon, New York, pp 49–68

    Google Scholar 

  • Osborne NN (1988) Retinal serotonin and the co-occurence of serotonin with other neurotransmitters. In: Osborne NN, Hamon M (eds) Neuronal serotonin. Wiley, Chichester, pp 129–152

    Google Scholar 

  • Pandey A, Habibulla M (1980) Serotonin in the central nervous system of the cockroach, Periplaneta americana. J Insect Physiol 26:1–6

    Google Scholar 

  • Pasik P, Pasik T, Saavedra JP (1982) Immunocytochemical localization of serotonin at the ultrastructural level. J Histochem Cytochem 30:760–764

    Google Scholar 

  • Pelletier G, Steinbusch HWM, Verhofstad AAJ (1981) Immunoreactive substance P and serotonin present in the same dense-core vesicles. Nature 293:71–72

    Google Scholar 

  • Rehder V, Bicker G, Hammer M (1987) Serotonin-immunoreactive neurons in the antennal lobes and suboesophageal ganglion of the honeybee. Cell Tissue Res 247:59–66

    Google Scholar 

  • Salecker I (1990) Deutocerebral serotonin-immunoreactive neurons in the brain of the American cockroach Periplaneta americana. In: Elsner N, Roth G (eds) Brain perception cognition. Proceedings of the 18th Göttingen Neurobiology Conference. Thieme, Stuttgart (no. 298)

    Google Scholar 

  • Schürmann FW, Klemm N (1984) Serotonin-immunoreactive neurons in the brain of the honeybee. J Comp Neurol 225:570–580

    Google Scholar 

  • Schürmann FW, Elekes K (1987) Synaptic connectivity in the mushroom bodies of the honeybee brain: electron microscopy and immunocytochemistry of neuroactive compounds: In: Menzel R, Mercer AR (eds) Neurobiology and behavior of honeybees. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Soghomonian JJ, Beaudet A, Descarries L (1988) Ultrastructural relationships of central serotonin neurons. In: Osborne NN, Hamon M (eds) Neuronal serotonin. Wiley, Chichester, pp 57–92

    Google Scholar 

  • Steinbusch HWM, Verhofstad AAJ, Joosten HWJ (1978) Localization of serotonin in the central nervous system by immunohistochemistry: description of a specific and sensitive technique and some applications. Neuroscience 3:811–819

    Google Scholar 

  • Steinbusch HWM, Verhofstad AAJ, Joosten HWJ (1982) Antibodies to serotonin for neuroimmunocytochemical studies. J Histochem Cytochem 30:756–759

    Google Scholar 

  • Steinbusch HWM, Tilders F (1987) Immunohistochemical techniques for light-microscopical localization of dopamine, noradrenaline, adrenaline, serotonin and histamine in the central nervous system. In: Steinbusch HWM (ed) Monoaminergic neurons: light microscopy and ultrastructure. Wiley, Chichester, pp 125–166

    Google Scholar 

  • Sternberger LA (1979) Immunocytochemistry, 2nd edn. Wiley, New York

    Google Scholar 

  • Tyrer NM, Turner JD, Altman JS (1984) Identifiable neurons in the locust central nervous system that react with antibodies to serotonin. J Comp Neurol 227:313–330

    Google Scholar 

  • Wässle H, Chun MH (1989) GABA-like immunoreactivity in the cat retina: light microscopy. J Comp Neurol 279:43–54

    Google Scholar 

  • Waldrop B, Christensen TA, Hildebrand JG (1987) GABA-mediated synaptic inhibition of projection neurons in the antennal lobes of the sphinx moth Manduca sexta. J Comp Physiol [A] 161:23–33

    Google Scholar 

  • Waldrop B, Hildebrand JG (1989) Physiology and pharmacology of acetylcholinergic responses of interneurons in the antennal lobes of the moth Manduca sexta. J Comp Physiol [A] 154:433–441

    Google Scholar 

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Salecker, I., Distler, P. Serotonin-immunoreactive neurons in the antennal lobes of the American cockroach Periplaneta americana: light- and electron-microscopic observations. Histochemistry 94, 463–473 (1990). https://doi.org/10.1007/BF00272608

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